Ultrastructure and wear patterns of the ventral epidermis of four snake species (Squamata,Serpentes)

Snakes are limbless tetrapods highly specialized for sliding locomotion. This locomotion leads to the skin being exposed to friction loads, especially on the ventral body side, which leads to wear. It is presumed that snakes therefore have specific optimizations for minimizing abrasion. Scales from snakes with habitat, locomotor and/or behavior specializations have specific gradients in material properties that may be due to different epidermal architecture. To approach this issue we examined the skin of Lampropeltis getula californiae (terrestrial), Epicrates cenchria cenchria (generalist), Morelia viridis (arboreal), and Gongylophis colubrinus (burrowing) with a focus on (i) the ultrastructure of the ventral epidermis and (ii) the qualitative abrasion pattern of the ventral scales. Scanning and transmission electron microscopy revealed variations in the structure, thickness, layering, and material composition of the epidermis between the species. Furthermore, SEM and white light interferometer images of the scale surface showed that the abrasion patterns differed, even when the snakes were reared on the same substrate. These data support the idea that (i) a specific gradient in material properties may be due to a variation in epidermis architecture (thickness/ultrastructure) and (ii) this variation may be an optimization of material properties for specific ways of life.     

Complete mitochondrial genome of the black-headed snake Sibynophis collaris (Squamata, Serpentes, Colubridae)

The black-headed snake Sibynophis collaris (Reptilia, Squamata, Colubridae) is a least concern species in the world. Two universal and two specific polymerase chain reaction (PCR) primers were used for long PCRs to amplify the whole mitochondrial genome of S. collaris. The products were subjected to do sequencing reactions. The complete genome is 17,163 bp in size, containing 37 genes coding for 13 proteins, 2 rRNAs, 22 tRNAs, and 2 control regions (CRI and CRII). The results could play an important role in the preservation of genetic resources for helping conservation of the endangered species.     

A new nematode (Nematoda: Cosmocercidae) from the lizard, Chamaeleo inturensis (Squamata: Chamaeleonidae) from the Democratic Republic of Congo

Maracaya africana n. sp. (Nematoda: Cosmocercidae) from the large intestine of the lizard Chamaeleo inturensis collected in Democratic Republic of Congo is described and illustrated. This is the first record of a species of Maracaya Diaz-Ungria (1963) for Africa. Light microscopy and scanning electron microscopy (SEM) studies revealed morphological differences in the structure of the male caudal end and cephalic end, which enabled us to differentiate these new species from the others. A key for determination of all species in the genus is provided.     

Alpine–Himalayan orogeny drove correlated morphological,molecular, and ecological diversification in the Persian dwarf snake (Squamata: Serpentes: Eirenis persicus)

The Persian dwarf snake Eirenis (Pseudocyclophis) persicus (Anderson, 1872) has a wide distribution range in south‐western Asia. This species group was comprehensively studied here using traditional biometry, geometric morphometrics, ecological niche modelling, and genetics. Our analyses revealed that E. persicus is split into two clades. A western clade, bearing at least two different species: E. persicus, distributed in south‐western Iran, and an undescribed species from south‐eastern Turkey and western Iran. The eastern clade consists of at least three species: Eirenis nigrofasciatus, distributed across north‐eastern Iraq, and western and southern Iran; Eirenis walteri, distributed across eastern Iran, southern Turkmenistan, and western and southern Pakistan, and Eirenis angusticeps, distributed in north‐eastern Pakistan. Ecological niche modelling revealed that the distribution of the species in the western clade are mainly affected by winter precipitation, and those in the eastern clade are mainly affected by the minimum temperature of the coldest month. A molecular clock analysis revealed that the divergence and diversification of the E. persicus species group mainly correspond to Eocene to Pliocene orogeny events subsequent to the Arabia–Eurasia collision. This study confirms that specimens with the unique morphology of having 13 dorsal scale rows on the anterior dorsum, occurring in the Suleiman Mountains in central Pakistan, can be referred to Eirenis mcmahoni (Wall, 1911). However, at this moment we have insufficient data to evaluate the taxonomy of this species.     

Placentation in the Mexican lizard Sceloporus mucronatus (Squamata: Phrynosomatidae)

We used light microscopy to study placental structure of the lizard Sceloporus mucronatus throughout 6 months of embryonic development. Three stages of placental development could be assigned to embryos based on the arrangement of the extraembryonic membranes. A highly vascular choriovitelline placenta was present in the embryonic hemisphere and a nonvascular bilaminar omphalopleure covered most of the abembryonic hemisphere of the egg during embryonic Stages 10-28. A chorioallantoic placenta replaced the choriovitelline placenta by embryonic Stage 29 and an omphaloplacenta covered the abembryonic hemisphere at this stage. The combination of these two placental types occurred in Stage 29-36 embryos. The final stage of placentation, embryonic Stages 37-40, was characterized by an omphalallantoic placenta in the abembryonic hemisphere and a chorioallantoic placenta in the embryonic hemisphere of the egg. The choriovitelline and chorioallantoic placentae are well vascularized, with closely apposed maternal and embryonic blood vessels. These structures are the most likely sites of respiratory exchange. In contrast, the omphaloplacenta and omphalallantoic placentae contain cuboidal or columnar epithelia and these structures may function in histotrophic exchange. Placentation of S. mucronatus is similar to that of predominantly lecithotrophic species in other squamate lineages suggesting that the evolution of this placental morphology is a response to similar factors and is independent of phylogeny.     

A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes)

Despite their medical interest, the phylogeny of the snake family Viperidae remains inadequately understood. Previous studies have generally focused either on the pitvipers (Crotalinae) or on the Old World vipers (Viperinae), but there has been no comprehensive molecular study of the Viperidae as a whole, leaving the affinities of key taxa unresolved. Here, we infer the phylogenetic relationships among the extant genera of the Viperidae from the sequences of four mitochondrial genes (cytochrome b, NADH subunit 4, 16S and 12S rRNA). The results confirm Azemiops as the sister group of the Crotalinae, whereas Causus is nested within the Viperinae, and thus not a basal viperid or viperine. Relationships among the major clades of Viperinae remain poorly resolved despite increased sequence information compared to previous studies. Bayesian molecular dating in conjunction with dispersal-vicariance analysis suggests an early Tertiary origin in Asia for the crown group Viperidae, and rejects suggestions of a relatively recent, early to mid-Tertiary origin of the Caenophidia.     

Thermoregulatory movement patterns of the lizard Podarcis carbonelli (Lacertilia: Lacertidae)

Using video cameras and motion detection software, we examined sequential positions of the lizard Podarcis carbonelli in a temperature gradient to look for patterns in spatial and temporal thermoregulatory movements. As lizards shuttled between warm and cool areas, their movements were typically slow; punctuated by bursts of speed. The animals were relatively inactive when heating, moved almost continually when cooling, and spent less time heating than cooling. Traditional modeling techniques proved unsuccessful, so we assessed the movement patterns with nonlinear dynamical techniques. The shuttling frequency, and the pattern of velocity changes, both met the qualitative attributes (self similarity, strange attractors, and noisy power spectra) and the quantitative criteria (positive Lyapunov exponent and capacity and/or correlation dimensions less than 5) that suggest deterministic chaos. These movement patterns appear regular, but at unpredictable times the patterns become disturbed before returning to regulation. There are both behavioral and physiological advantages to movements that follow a model of deterministic chaos control.     

A tiny lizard (Lepidosauria,Squamata) from the Lower Cretaceous of Spain

Abstract: The smallest living amniotes are all lizards, but the fossil history of this size trait in Squamata is difficult to follow because small skeletons have low preservation potential and are often hard to detect in the field. A new squamate taxon, Jucaraseps grandipes gen. et sp. nov., is here described on the basis of an articulated skeleton from the Early Cretaceous Spanish lagerstätten of Las Hoyas. It differs from other known Mesozoic lizards in combining very small body size with a short rostrum, low maxillary tooth count, a relatively slender and elongated body, and short limbs with large hind feet. Phylogenetic analysis using TNT places it on the stem of a clade encompassing scincomorphs, gekkotans, snakes, amphisbaenians and anguimorphs. Comparison with modern lizards suggests it was probably a cryptic surface or subsurface ground dweller but not a burrower.     

Novel placental structure in the Mexican gerrhonotine lizard,Mesaspis viridiflava (Lacertilia; Anguidae)

The evolution of viviparity alters the physical relationship between mothers and offspring and the prevalence of viviparity among squamate reptiles presents an opportunity to uncover patterns in the evolution of placental structure. Understanding the breadth of this diversity is limited because studies of placental structure and function have emphasized a limited number of lineages. We studied placental ontogeny using light microscopy for an embryological series of the Mexican gerrhonotine lizard, Mesaspis viridiflava. This species develops an elaborate yolk sac placenta, an omphaloplacenta, which receives vascular support arising in a structure known only from other gerrhonotine lizards. A prominent feature of the omphaloplacenta is a zone of uterine and embryonic epithelial cell hyperplasia located at the upper shoulder of the yolk mass, often extending above the yolk mass. The omphaloplacenta covers more than one-half of the surface area of maternal—embryonic contact. The chorioallantoic placenta has a more restricted distribution because the allantois remains in the embryonic hemisphere of the egg throughout development and lies internal to the vascular support for the omphaloplacenta in areas where they overlap. The structural profile of the chorioallantoic placenta indicates a potential for respiratory exchange and/or hemotrophic nutritive transport, while that of the omphaloplacenta suggests that nutritive transfer is primarily via histotrophy. An eggshell is present in the earliest embryonic stages examined but regresses relatively early in development. Placental specializations of this species are consistent with a pattern of matrotrophic embryonic nutrition and have evolved in a unique lineage specific developmental pattern.     

Evolution of coloration, urotomy and coral snake mimicry in the snake genus Scaphiodontophis (Serpentes: Colubridae)

The Neotropical hinged-tooth, coral snake mimics of the genus Scaphiodontophis are characterized by extremely long and disproportionately thick tails that are extremely fragile. Both the coloration and tail structure are putative antipredator devices. While all examples have components of the coloration that match those of the venomous coral snakes (family Elapidae), the range of variation is extreme, leading to controversy on the status of various populations, including nine named taxa. Individual, ontogenetic and geographic variation in scutellation and head, body and tail coloration were analysed to evaluate population status and possible evolutionary trends based on a sample of 183 examples from Mexico, Central America and Colombia. Variation in subcaudal counts show population differences (higher in Mexico and upper Central America) but are not congruent with geographic variation in coloration. Generally snakes from north of Nicaragua and from central and eastern Panama have a pattern of dyads (black-light-black bands separating red bands), those from Atlantic slope Nicaragua to western Panama a pattern of monads (light-black-light bands separating the red ones) and those from Colombia have both pattern types on the same snake. The dyads and/or monads may be present the length of the body and tail, restricted to the anterior part of the body or on the entire body or on the anterior part of the body and on the tail. Two or more of these variants may occur at a single geographic locality or only a single one may be present. Head and nuchal colour patterns (Z, A, V and Du) are relatively consistent geographically. The Adantic slope Guatemala, Belize and Honduras population have the A pattern, those of Nicaragua, Costa Rica and western Panama the V pattern, and those in Colombia a Du pattern. Other populations have the Z coloration. Intermediate conditions in coloration of the body and tail and head and neck are found at localities intermediate between the main pattern types, indicating intergradation among adjacent populations. Consequently, we regard these snakes as representative of a single species, Scaphiodontophis annulatus Dumeril and Bibron and the eight other names applied to various populations and individuals as synonyms. Analysis of colour pattern leads us to the conclusion that the tricolour pattern evolved from a uniform one through a lineate-spotted condition (usually present on the non-tricolour portions of the snake) through a bicolour red and black pattern to the dyadal condition. The monadal pattern in turn was derived from the dyadal one. The data further indicates that tricolour components first appeared anteriorly and progressively expanded posteriorly. The evolutionary sequence for the head and nuchal pattern appears to be A → Z → V → Du S. annulatus has a series of jaw and tooth specializations designed for rapid processing of hard-bodied prey found during diurnal foraging in the leaf-litter. Urotomy in this species involves intervertebral tail-breakage (pseudoautotomy) without regeneration. Evidence is presented supporting the long-tail multiple break hypothesis as applicable to Scaphiodontophis and other snakes with similar tail morphology (specialized pseudoautotomy). This is in contrast to snakes with similar tail morphology (specialized pseudoautotomy). This is in contrast to Coniophanes and other snakes with a high incidence of urotomy having long but unspecialized tails (unspecialized pseudoautotomy) without multiple breaks over time. All Scaphiodontophis colour patterns have a general resemblance to that of venomous coral snakes and offer protection from generalizing predators having innate or other triggered responses to coral snake colours. The aposematic effect is enhanced by tail thrashing and head twitching behaviours. The characteristic foraging pose of S. annulatus, which tends to expose the head and anterior body, makes even the incomplete tricolour pattern effective as an antipredator defence. No evidence supports the idea that tail thrashing or the incomplete tricolour pattern directs the predator attacks to the tail to expedite pseudoautotomy. Coral snake mimicry and specialized pseudoautotomy are shown not to be co-evolved and pseudautotomy seems to have evolved long before mimetic coloration in this genus.     

Polymorphic microsatellite markers for the lizard Psammodromus algirus (Squamata: Lacertidae)

Eight microsatellite loci are described for the lizard Psammodromus algirus, a species widely used as a model in behavioural and ecological studies. All loci were highly polymorphic (six alleles or more per locus) in a sample of 24 individuals from a single site near Navacerrada (central Spain). Observed heterozygosity ranged from 0.29 to 0.96. These markers will be used to study mating strategies and determinants of reproductive success in this species.     

The embryonic development of the Egyptian cobra Naja h. haje (Squamata: Serpentes: Elapidae)

The Egyptian cobra, Naja h. haje, is the largest of the African cobras and is a member of a successful and medically important species complex found throughout Africa, north and south of the Sahara, as well as across the Arabian Peninsula to Oman. Although its phylogenetic position and venom characteristics have been well studied, its development has not. Here, we present a normal staging table for N. h. haje, based on external features. Comparison with firstly the Asian monocled cobra, Naja kaouthia, and then with the small number of other oviparous snake species, allowed us to examine whether differences between two species in the same genus were of the same type and magnitude as those between unrelated genera. In fact, at least with respect to external features, we found a similar level of disparity. N. h. haje embryos lagged behind those of N. kaouthia in body and head scale development, size in ovo and hatchling length, despite having a slightly shorter incubation period and a somewhat larger adult size. Some of these differences may have been the result of differing incubation temperatures. Nonetheless, there does appear to be a broadly conserved pattern of in ovo development in at least macrostomatan snakes.     

An unusual lizard (Reptilia: Squamata) from the Early Cretaceous of Las Hoyas, Spain

The Early Cretaceous (Barremian) lepidosaurian assemblage of Las Hoyas (Cuenca Province, Castilla-La Mancha), Spain, resembles that of roughly contemporaneous localities at Montsec (Catalonia), Una (Castilla-La Mancha) and Galve (Aragon) in being dominated by the scincomorph lizard Meyasaums ( Ilerdaesaurus ). It differs in the presence of two previously unknown taxa, one of which, described here, shows a strikingly unusual morphology in its ribs and distal limb skeleton suggestive of climbing specialization. This form is sufficiently distinct from other known taxa to warrant the erection of a new genus and species, Scandensia ciervensis gen. et sp. nov. Cladistic analysis of Scandensia suggests that it forms a sister taxon to living squamates (Iguania + Scleroglossa and all descendants of their most recent common ancestor).     

Postovipositional development of the sand snake Psammophis sibilans (Serpentes:Lamprophiidae) in comparison with other snake species

Characterizing and comparing developmental progress across different species helps to interpret how different or similar body forms evolved. We present an embryonic table for the oviparous African Sand Snake Psammophis sibilans from the Lamprophidae family, describing its postovipositional in ovo development. Psammophis is a good model of a genus that is widely distributed in Africa and Asia and includes 22 species. We describe ten embryonic stages based on the development of externally visible morphological characteristics such as; pharyngeal arches, facial processes, eyes, scales, body pigmentation and body colour pattern development. This study discusses the development of this snake and compares it with that of the closely related brown house snake Lamprophis fulliginosus (Lamprophidae) and the medically important venomous cobras Naja haje haje and Naja kaouthia from the sister lineage Elapidae. The distantly related basal snake Python sebae, which displays different morphology and behaviour, was chosen for deeper insight into the evolution of body structures within the snake clade. We found interspecific differences in the relative stage of development of embryonic structures at the time of oviposition and during postovipositional embryonic development. One of the outcomes of this study is that embryonic structures such as the pharyngeal processes, eye pigmentation and scales are interspecifically conservative in regard to timing of morphodifferentiation, while body pigmentation, colour and colour pattern are interspecifically plastic in their temporospatial development.     

Placental ontogeny of the Tasmanian scincid lizard, Niveoscincus ocellatus (Reptilia: Squamata)

A prominent scenario for the evolution of reptilian placentation infers that placentotrophy arose by gradual modification of a simple vascular chorioallantoic placenta to a complex structure with a specialized region for nutrient transfer. The structure of the chorioallantoic placenta of Niveoscincus ocellatus, apparently described originally from a single embryonic stage, was interpreted as a transitional evolutionary type that provided support for the model. Recently, N. ocellatus has been found to be as placentotrophic as species with complex chorioallantoic placentae containing a specialized region called a placentome. We studied placental development in N. ocellatus and confirmed that the chorioallantoic placenta lacks specializations found in species with a placentome. We also found that this species has a specialized omphaloplacenta. The chorioallantoic placenta is confined to the region adjacent to the embryo by a membrane, similar to that found in some other viviparous skinks, that divides the egg into embryonic and abembryonic hemispheres. We term this structure the "inter-omphalopleuric" membrane. The position of this membrane in N. ocellatus is closer to the embryonic pole of the egg than to the abembryonic pole and thus the surface area of the omphaloplacenta is greater than that of the chorioallantoic placenta. In addition, the omphaloplacenta is regionally diversified and more complex histologically than the chorioallantoic placenta. An impressive and unusual feature of the omphaloplacenta of N. ocellatus is the development of extensive overlapping folds in the embryonic component of mid-gestation embryos. The histological complexity and extensive folding of the omphaloplacenta make this a likely site of placental transfer of nutrients in this species.     

The first known chamopsiid lizard (Squamata) from the Upper Cretaceous of Europe (Csehbánya Formation; Hungary,Bakony Mts)

The Upper Cretaceous (Santonian) Iharkút terrestrial vertebrate locality, in Hungary, has yielded several lacertilian taxa since its discovery in 2000. One of these is represented by a left mandible fragment and two dentary fragments. The characters observed on these remains support assignment to the family Chamopsiidae (Scincomorpha). Moreover, the remains belong to a new genus and species, Pelsochamops infrequens n. g. n. sp. Pelsochamops is the first known occurrence of chamopsiids outside North America and adds another scincomorphan lizard to the Iharkút fauna. It represents an additional evidence for dispersal routes between North America and Europe.     

Interembryonic regions of the uterus of the viviparous lizard Mabuya brachypoda (Squamata: Scincidae)

Analysis of the structure and physiology of the uterine incubation chambers of viviparous squamates has provided insight concerning adaptations for gestation. However, the literature addressing the biology of the interembryonic regions of the uterus is very limited, presumably because it has been assumed that this area has little role in the development and support of embryos in viviparous squamates. This study was undertaken to examine the histology of the interembryonic regions of Mabuya brachypoda, a viviparous lizard with microlecithal ova and consequently substantial matrotrophic activity. The incubation chambers are oval, distended zones of the uterus, adjacent to the interembryonic regions. The wall of the interembryonic regions includes: mucosa, formed by a cuboidal or columnar epithelium with ciliated and nonciliated cells, and a lamina propria of vascularized connective tissue containing abundant acinar glands; myometrial smooth muscle consisting of inner circular and outer longitudinal layers; and serosa. The segment of the interembryonic region adjacent to the incubation chamber forms a transitional segment that displays folds of the mucosa that protrude into the uterine lumen. The limit of the incubation chamber is well defined by the long mucosal folds of the transitional segment. Long and thin extensions of extraembryonic membranes are present in the lumen of the transitional segment, outside of the incubation chamber region. The presence of abundant uterine glands and extraembryonic membranes in the interembryonic regions during gestation suggests uterine secretory activity and histotrophic transfer of nutrients to embryos in these regions.